Adverse Impact of Intraoperative Conversion on the Postoperative Course Following Laparoscopic Pancreaticoduodenectomy - Yonsei Medical Journal

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Original Article
                      Yonsei Med J 2021 Sep;62(9):836-842
                      https://doi.org/10.3349/ymj.2021.62.9.836                                                                pISSN: 0513-5796 · eISSN: 1976-2437

Adverse Impact of Intraoperative Conversion
on the Postoperative Course Following
Laparoscopic Pancreaticoduodenectomy
Law Cho Kwan Connie1*, Seung Soo Hong2,3*, Incheon Kang4, Seung Yoon Rho5,
Ho Kyoung Hwang2,3, Woo Jung Lee2,3, and Chang Moo Kang2,3
1
 Department of General Surgery, Tuen Mun Hospital, Hong Kong SAR, China;
2
 Division of Hepatobiliary and Pancreatic Surgery, Department of Surgery, Yonsei University College of Medicine, Seoul;
3
 Pancreatobiliary Cancer Center, Yonsei Cancer Center, Severance Hospital, Seoul;
4
 Division of Hepatobiliary and Pancreatic Surgery, Department of Surgery, CHA Bundang Medical Center, CHA University, Seongnam;
5
 Division of Hepatobiliary and Pancreatic Surgery, Department of Surgery, Yongin Severance Hospital, Yongin, Korea.

Purpose: The aim of the current study was to evaluate the adverse clinical impact of intraoperative conversion during laparo-
scopic pancreaticoduodenectomy (LPD).
Materials and Methods: The medical records of patients who underwent pancreaticoduodenectomy (PD) were retrospectively
reviewed. Perioperative clinical variables were compared between patients who underwent converted PD (cPD) and initially
planned open PD (OPD) to investigate the clinical impact and predictive factors of intraoperative conversion during LPD.
Results: A total of 171 patients were included. Among them, 31 patients (19.3%) were found to have intraoperative conversion dur-
ing LPD. Failure of progression due to severe adhesion (12 patients, 7%) and major vessel invasion (7 patients, 4%) were the two
most frequent reasons for conversion. On multivariate analysis, age [Exp(β)=1.044, p=0.044] and pancreatic texture [Expa(β)=2.431,
p=0.039) were found to be independent factors for predicting intraoperative conversion during LPD. In comparative analysis with
the OPD group, the cPD group had a longer operation time (516.8 min vs. 449.9 min, p=0.001), higher rate of postoperative hem-
orrhage (12.1% vs. 0.85%, p=0.008), higher reoperation rate (9.1% vs. 0%, p=0.01), and higher cost (21886.4 USD vs. 17168.9 USD,
p=0.018).
Conclusion: Intraoperative conversion during LPD can have an adverse clinical impact on the postoperative course following
LPD. Appropriate patients selection and improvement of surgical techniques will be crucial for unnecessary intraoperative con-
version and safe LPD.

Key Words: ‌Laparoscopic, pancreaticoduodenectomy, conversion, complication, morbidity

INTRODUCTION                                                                          ner and Pomp1 reported the first experience of LPD in 1994,
                                                                                      LPD has been regarded as a technically feasible and safe sur-
Laparoscopic pancreaticoduodenectomy (LPD) is a complicat-                            gery by hepatobiliary and pancreas experts. Recently, more en-
ed and technically demanding surgical procedure. Since Gag-                           couraging perioperative outcomes of LPD have been reported,
Received: December 17, 2020 Revised: June 24, 2021 Accepted: June 28, 2021
Corresponding author: Chang Moo Kang, MD, PhD, Division of Hepatobiliary and Pancreatic Surgery, Department of Surgery, Yonsei University College of Medicine, 50-1
Yonsei-ro, Seodaemun-gu, Seoul 03722, Korea.
Tel: 82-2-2228-2135, Fax: 82-2-313-8289, E-mail: cmkang@yuhs.ac
*Law Cho Kwan Connie and Seung Soo Hong contributed equally to this work.
•The authors have no potential conflicts of interest to disclose.
© Copyright: Yonsei University College of Medicine 2021
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0)
which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

836                                                                                                                                                www.eymj.org
Law Cho Kwan Connie, et al.

compared with open PD (OPD) in treating periampullary tu-             erative radiological images. Initial OPD was indicated when
mors.2-6 Recently, the PADULAP randomized control trial dem-          patients who refused to have LPD, and they had tumor condi-
onstrated that LPD was associated with a significantly lower          tions expected to undergo intraoperative conversion, such as
duration of hospital stay and fewer Clavien-Dindo grade ≥3 com-       high risk of tumor invasion around the major vascular struc-
plications, while the resection margin and lymph node harvest         tures, and severe intraabdominal adhesion. Intraoperative con-
were comparable.7 The meta-analysis by Chen, et al.8 also showed      version was defined as resection that had to be completed by
that LPD had lower transfusion rates, shorter hospital stay, and      laparotomy due to technical difficulties or failure to progress
less blood loss. However, in general, the technical feasibility and   during LPD. The primary end point of this study was to evalu-
safety of LPD still remain controversial.1,9                          ate the perioperative adverse impacts of unplanned intraop-
   The inflammatory response secondary to obstructive chol-           erative conversion during LPD (cPD) by comparative analysis
angitis and pancreatitis can cause dense adhesion and unex-           with initial OPD. The costs associated with unplanned conver-
pected local invasion of the tumor into major vessels, which do       sion were also compared.
not favor safe and effective laparoscopic dissection. In addition,
laparoscopic management of the soft remnant pancreas with             Data collection
small pancreatic duct is difficult, and these conditions are clin-    The patients’ demographic parameters, including age, Ameri-
ically relevant to the development of a postoperative pancreatic      can Society of Anesthesiologists (ASA) physical status, body
fistula (POPF).10,11 Indeed, POPF can be a critical complication      mass index (BMI), and neoadjuvant therapy, were evaluated.
after pancreatectomy, and it was reported to occur in 3.8%–50%        The reoperation rate, readmission rate, postoperative hemor-
of cases in previous meta-analyses.2,3,12-14 Therefore, performing    rhage rate, occurrence of delay gastric emptying and POPF (de-
safe LPD to minimize postoperative morbidity is a major con-          fined by the International Study Group on Pancreatic Fistula,
cern in reconstruction during LPD. Certain intraoperative cir-        ISGPF),22 30-day mortality, and morbidities were assessed. Fur-
cumstances leading to difficult laparoscopic dissection and re-       thermore, the transfusion rate, short-term surgical outcome (in-
constructions are considered main reasons for intraoperative          cluding transfusion rate), number of retrieved lymph nodes, and
conversion during LPD.                                                R-status of the resection specimen were also evaluated. In addi-
   Intraoperative conversion to OPD (converted PD, cPD) is a          tion, we examined the reasons for unplanned conversion, such
practical issue for both pancreatic surgeons and patients. PD is      as major vascular invasion, failure to progress due to adhesion,
a very complicated surgical procedure, and timely intraopera-         easy bleeding tendency, and anatomical anomalies. The Insti-
tive conversion is essential to ensure the safety of LPD. Howev-      tutional Review Board of Severance Hospital approved this study
er, several previous reports lacked specific data on intraopera-      protocol (IRB No. 4-2018-0863).
tive conversion during LPD.2,3,7,15 According to literature, it is
estimated that the overall conversion rate during LPD is 3.1%–        Surgical procedure
24.1% in experienced surgeons.16-21 However, few studies have         During LPD, the resection and reconstruction of pancreatico-
investigated the potential impact of intraoperative conversion        jejunostomy and hepaticojejunostomy were performed intra-
during LPD on the perioperative clinical course.                      corporeally. The surgical specimen was retrieved through a mini-
   In this study, the perioperative clinical impact of intraoper-     laparotomy wound by extending the umbilical port site where
ative conversion during LPD was evaluated, and the potential          the duodenojejunostomy was performed.5,23-25
predictive factors for intraoperative conversion were also inves-
tigated. This study is expected to assist in selecting appropriate    Statistical analysis
patients to avoid unnecessary intraoperative conversion and           Continuous variables were described as the mean±standard de-
achieve the goal of safe LPD.                                         viation, and categorical variables were described as the frequen-
                                                                      cy (%). Categorical variables were analyzed using the chi-squared
                                                                      test, and the Student’s t-test was used for continuous variables.
MATERIALS AND METHODS                                                 To identify the predictive factors for conversion, multivariate
                                                                      analyses were performed for different variables using a logistic
Study design                                                          regression model. p-values
Conversion in Lap PPPD

formed; 93 patients were male and 78 patients were female, with                   42.8%, chi-square, Fisher’s exact test, linear-to-linear associa-
an age range of 61.1±12.0 years. Among them, 155 patients (91%)                   tion, p=0.013) (Fig. 1).
underwent laparoscopic pylorus-preserving pancreaticoduo-                            Failure of dissection due to severe adhesion was the most
denectomy (Lap-PPPD), 15 patients (9%) underwent laparo-                          common reason for conversion during LPD (12 patients, 38.7%),
scopic total pancreatectomies (Lap-TP), and 1 patient (0.6%)                      followed by suspicion of major vessel [superior mesenteric vein
underwent conventional pancreaticoduodenectomy (Lap-PD).                          (SMV)/portal vein (PV)] invasion (7 patients, 22.5%) (Table 2).
Only 4 patients (2%) received neoadjuvant therapy before surgery.                 The main reasons for adhesion were severe inflammation due
  Over 70% of the surgeries were performed for malignant dis-                     to cholangitis, pancreatitis, post neoadjuvant therapy, desmo-
eases. Among these, common bile duct cancer was the most                          plastic changes surrounding pancreatic head, and direct tumor
common (40 patients, 23%), followed by the ampulla of Vater                       invasion to major vasculatures. In addition, combined segmen-
cancer (35 patients, 20%). In benign and low-grade malignant                      tal resection of the colon was necessary in two conversion cases
tumors of the pancreas, intraductal papillary mucinous neo-                       due to incidental ischemic change of colon following excision
plasms were the most common (26 patients, 15%) (Table 1).                         or shaving of colonic mesentery for tumor invasion.

Incidence and reasons for intraoperative conversion                               Predictive factors for intraoperative conversion
during LPD                                                                        during LPD
Among the 171 attempted LPDs, 31 patients had to convert to                       In univariate analysis, age (p=0.013), sex (p=0.019), ASA physi-
an open approach during LPD (cPD) and the overall conver-                         cal status (p=0.039), total bilirubin (p=0.06), size of the pancre-
sion rate was 19.3%. Moreover, the intraoperative conversion                      atic duct (p=0.047), and pancreatic texture (p=0.015) were as-
rate during LPD was found to be steady over time (range, 13.3%–                   sociated with conversion during LPD. Diagnosis, neoadjuvant
                                                                                  therapy, BMI, and the size of bile duct were not found to be re-
Table 1. Diagnosis in 171 Laparoscopic Pancreaticoduodenectomy
Cases
                                                                                  lated to conversion (p>0.05) (Table 3). On multivariate analysis,
                                                                                  age {Exp(β)=1.044 [95% confidence interval (CI): 1.001–5.660],
CBD cancer                                      40 (23)
                                                                                  p=0.044} and pancreatic texture [hard pancreas; Exp(β)=2.431
AoV cancer                                      35 (20)
                                                                                  (95% CI: 1.044–5.660), p=0.039] were found to be independent
PDAC                                            29 (17)
IPMN                                            26 (15)                           Table 2. Reasons for Conversion during Lap-PD
Metastatic cancer                                15 (9)
                                                                                                Reasons for conversion                         Frequency (%)
NET                                              14 (8)
                                                                                  Failure to progress due to severe adhesion                        12 (39)
AoV adenoma                                      10 (6)
                                                                                  Suspicious SMV/PV invasion                                         7 (23)
SPN                                              6 (4)
                                                                                  Hepatic artery invasion                                            3 (9.6)
GIST                                             5 (3)
                                                                                  Combined colon segmental resection                                 2 (6.4)
Duodenal cancer                                 4 (0.6)
                                                                                  Internal obesity                                                   2 (6.4)
SCN                                              2 (1)
                                                                                  Consecutive positive bile duct resection margin                    2 (6.4)
Pancreatitis                                    1 (0.5)
                                                                                  Sustained high pCO2                                                2 (6.4)
Ganglioma                                       1 (0.5)
                                                                                  Vascular anomaly (RHA penetrating pancreatic head)                 1 (
Law Cho Kwan Connie, et al.

Table 3. Clinically Detectable Factors Associated with Converting PD         Table 5. Demographics between Converting PD and Initial Open PD
                             Successful LPD Converting PD                                                Converting PD     Initial open PD
                                                                p value                                                                    p value
                                (n=138)        (n=33)                                                       (n=33)              (n=117)
Age (yr)                       59.9±12.1      65.7±10.9           0.013      Age (yr)                      65.7±10.9          64.1±9.9      0.392
Sex (male/female)                69/69           24/9             0.019      Sex (male/female)                24/9               71/46      0.227
Diagnosis 1 (benign &                                                        Diagnosis 1 (benign &
                                   50/88           9/24           0.609                                         9/24            9/108          0.017
 low-grade/malignant)                                                         low-grade/malignant)
Diagnosis 2 (PC/non-PC)           21/117            8/25          0.215      Diagnosis 2 (PC/non-PC)            8/25            52/65          0.044
ASA (1/2)                          13/77            0/17          0.039      ASA (1/2/3/4)                   0/17/15/1        7/53/51/6        0.882
ASA (3/4)                           48/0            15/1                     Neo-Tx (no/yes)                    32/1            94/23          0.028
Neo-Tx (no/yes)                    135/3            32/1          0.579      Total bilirubin                  1.4±1.1          1.3±1.2         0.631
Total bilirubin                   1.0±0.9          1.41.1         0.076      BMI                             23.0±2.5         23.3±3.1         0.744
BMI                              23.5±2.9        23.0±2.5         0.431      Operating time                516.8±96.6        449.9±102.9       0.001
BD-size                           1.2±1.0        1.3±0.5          0.403      EBL                           645.5±559.4       562.1±439.2       0.368
PD-size                           3.6±2.2         4.8±3.1         0.047      Transfusion (no/yes)               30/3           102/15          0.764
Pancreatic texture                                                           Tumor size                       3.4±2.1          2.9±1.6         0.224
                                   96/30           16/14          0.015
 (soft/hard)                                                                 No. of retrieved LNs            12.4±7.5         13.9±8.9         0.380
PD, pancreaticoduodenectomy; LPD, laparoscopic pancreaticoduodenectomy;      No. of metastatic LNs            1.9±2.8          1.6±2.9         0.522
PC, pancreatic cancer; ASA, American Society of Anesthesiologists; Neo-Tx,   R-status                           0/33            4/111          0.575
neoadjuvant treatment; BMI, body mass index; BD-size, bile duct size; PD-
size, pancreatic duct size.                                                  PC, pancreatic cancer; ASA, American Society of Anesthesiologists; Neo-Tx,
                                                                             neoadjuvant treatment; BMI, body mass index; PD, pancreaticoduodenecto-
Table 4. Preoperatively Detectable Clinical Factors Associated with          my; EBL, estimated blood loss; LN, lymph nodes.
Hard Remnant Pancreas*
                              Soft pancreas   Hard pancreas                  Table 6. Adverse Impact of Converting PD on Postoperative Course
                                                            p value
                                 (n=112)          (n=44)                                                  Converting PD Initial open PD
                                                                                                                                               p value
Age (yr)                        59.8±12.1       64.1±11.1    0.041                                            (n=33)            (n= 117)
Sex (male/female)                  60/52           27/17     0.474           POPF (no/yes)                     28/5              98/19          0.463
Diagnosis 1 (benign &                                                        POBF (no/yes)                     32/1              113/4          1.000
                               7/34/71             0/7/37         0.024
 low-grade/malignant)                                                        DGE (no/yes)                      26/7              99/18          0.598
Diagnosis 2 (PC/non-PC)         11/101             17/44
Conversion in Lap PPPD

three units of packed red blood cells during the postoperative        19.6%, and the morbidity was significantly higher, especially in
period. The other two patients were associated with POPF, which       terms of wound infection and longer hospital stay. In contrast,
required interventional angiography and embolization. An-             the study by Casillas, et al.28 showed no significant differences in
other patient required reoperation for bleeding from the liver        operative time, length of stay, costs, or unexpected remissions.
bed due to detachment of the gallbladder. It was also observed           Despite these previous studies, the impact of intraoperative
that emergent diverting loop ileostomy was required in a case         conversion during LPD has not been fully investigated. Recent-
of combined colon resection during cPD, and secondary wound           ly, Torphy, et al.16 evaluated the clinical impact of conversion to
closure was necessary in one patient. Finally, the medical cost       the open approach in their subgroup analysis of minimally in-
was reported to be much higher in the conversion group than           vasive PD. They found that 84 robotic pancreaticoduodenecto-
in the initial OPD group {24591443±11903768.2 (₩) [21886.4±           mies (RPD, 15.3%) and 823 LPD (25.7%) were converted to OPD.
10594.4 ($)] vs. 19290897.2±5587761.9 (₩) [17168.9±4973.1 ($)];       The LPD patients requiring conversion had no significant dif-
p=0.018} (Table 6).                                                   ferences in terms of 90-day mortality compared to those who
                                                                      completed LPD [odds ratio (OR), 1.48; 95% CI, 0.97–2.24]. For
                                                                      RPD, while the conversion group showed a 4-fold increase in
DISCUSSION                                                            90-day mortality, no significant difference observed in the con-
                                                                      version rate over time (p=0.605). Furthermore, the lower the
Since the first LPD was performed in 2008 in our center, the an-      volume of minimally invasive PD centers, the higher the con-
nual number of LPD has steadily increased. However, the over-         version rate; therefore, the conversion group likely had longer
all conversion rate was estimated to be 19.3% in this study, which    operative times and more blood loss. A recent multicenter study29
is similar to that in other studies. To the best of our knowledge,    found that elective conversion (e.g., vascular involvement) in
no previous study has directly compared perioperative outcomes        minimally invasive distal pancreatectomy for pancreatic ductal
between cPD and initial OPD to investigate the potential clini-       adenocarcinoma was associated with comparable short-term
cal impact of cPD. Therefore, this study is thought to be the first   oncological outcomes to OPD, while emergency conversions
to investigate the potential adverse impact of conversion during      (e.g., bleeding) were associated with worse outcomes over both
LPD. In this study, the conversion group had a longer operating       short and long terms. This finding suggests that careful patient
time, higher occurrence of postoperative hemorrhage, higher           selection and timely conversion are required to safely conduct
reoperation rate, and consequently higher medical costs. For the      minimally invasive pancreatectomy.
patients’ safety during LPD, unnecessary intraoperative con-             The current study shows that both age and pancreatic texture
version during LPD should be avoided. This can be ensured by          were independent factors that could predict conversion during
careful preoperative patient selection. Therefore, prediction of      LPD. Practically, pancreatic texture (hard pancreas) can be pre-
the potential risk of intraoperative conversion before surgery        dicted by pancreatic duct size [Exp(β)=1.473 (95% CI: 1.234–
is important.                                                         1.758), p
Law Cho Kwan Connie, et al.

abutted SMV/PV in preoperative CT scan. At present, it is con-        a growing number of pancreatic surgeons are performing lap-
sidered impossible to fully predict the possibility of laparoscop-    aroscopic or even RPD. A multicenter collaborative study would
ic resection through preoperative image studies. However, the         be worthwhile to justify the safety of unplanned conversion to
common point of open conversion cases is that all of the patients     open surgery for minimally invasive LPD performed by differ-
have undergone biopsy of the tumor via EUS or endoscopic ret-         ent surgeons, and to prevent its adverse effects.
rograde cholangiopancreatography, which can result in tissue
injury and inflammation. The adhesion due to inflammation             AUTHOR CONTRIBUTIONS
can mimic tumor invasion to the major vessels. It is recommend-
ed to avoid unnecessary biopsy for lesions requiring surgical         Conceptualization: Chang Moo Kang. Data curation: Law Cho Kwan
excision regardless of the biopsy results.                            Connie and Seung Soo Hong. Formal analysis: Law Cho Kwan Con-
                                                                      nie and Seung Soo Hong. Investigation: Incheon Kang and Seung
   Torphy, et al.16 mainly reported factors associated with a high-
                                                                      Yoon Rho. Methodology: Incheon Kang and Seung Yoon Rho. Project
er risk of conversion in a minimally invasive group; these includ-    administration: Ho Kyoung Hwang and Woo Jung Lee. Resources: Ho
ed the male sex, tumor size >34 mm, and a low PD volume cen-          Kyoung Hwang and Woo Jung Lee. Software: Ho Kyoung Hwang and
ter. In this study, the patients’ BMI was around 23 kg/m2, which      Woo Jung Lee. Supervision: Chang Moo Kang. Validation: Chang Moo
was not associated with conversion during LPD (23.0±2.5 vs.           Kang. Visualization: Law Cho Kwan Connie and Seung Soo Hong.
                                                                      Writing—original draft: Law Cho Kwan Connie and Seung Soo Hong.
23.3±3.1, p=0.744). However, Cesaretti, et al.31 recommended that
                                                                      Writing—review & editing: Law Cho Kwan Connie, Seung Soo Hong,
patients with a BMI >40 m/kg2 and locally advanced lesions            and Chang Moo Kang. Approval of final manuscript: all authors.
should be reconsidered for LPD. Although the present study
failed to reveal the impact of BMI on intraoperative conversion,
                                                                      ORCID iDs
according to our experiences, in patients with high BMI, it was
difficult to ensure an operative field, especially when dissecting    Law Cho Kwan Connie        https://orcid.org/0000-0001-5498-8833
uncinate processes due to the bulky omentum and colon hiding          Seung Soo Hong             https://orcid.org/0000-0001-9913-8437
in this area, which make the surgery very difficult. In particular,   Incheon Kang               https://orcid.org/0000-0003-4236-5094
this area, known as the retroperitoneal margin (SMA lateral mar-      Seung Yoon Rho             https://orcid.org/0000-0002-1265-826X
                                                                      Ho Kyoung Hwang            https://orcid.org/0000-0003-4064-7776
gin), is oncologically very important in patients with pancre-        Woo Jung Lee               https://orcid.org/0000-0001-9273-261X
atic cancer. Therefore, BMI should also be considered as one of       Chang Moo Kang             https://orcid.org/0000-0002-5382-4658
the preoperative selection criteria for LPD. In the near future,
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https://doi.org/10.3349/ymj.2021.62.9.836                                                                                                841
Conversion in Lap PPPD

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